BRAZILIAN JOURNAL OF OCEANOGRAPHY, 59(2):145-152, 2011

TEMPORAL VARIATION IN VEGETATIVE DEVELOPMENT OF scalpelliformis () FROM BALEIA BEACH, ILHA GRANDE BAY (RIO DE JANEIRO, BRAZIL)

Marcelo Augusto Vasconcelos 1, Carolina Leite Queiroga Schubart 2 and Maria Teresa Menezes de Széchy 1*

1Universidade Federal do Rio de Janeiro – Instituto de Biologia Departamento de Botânica (Rua Professor Rodolpho P. Roço, 211, sala A-99, 21941-902 Ilha do Fundão, RJ, Brasil)

2Associação Nacional dos Fiscais Federais do Meio Ambiente (Ed. Porto do Lago, Lago Norte, Brasília, DF, Brasil)

*Corresponding author: [email protected]

A B S T R A C T

Caulerpa scalpelliformis grows on rocky and sandy bottoms at different depths in Jacuacanga Cove, Ilha Grande Bay, where it can form dense patches. The invasive behavior of this and other species of Caulerpa is well documented in the literature. This study analyzed the variation of the vegetative development of C. scalpelliformis from Baleia Beach (23°01’63’’S and 44°14’18’’W) in Jacuacanga Cove, from June 2003 to September 2004, including plants from rocky and sandy substrates. Morphometric and dry weight data from the erect and prostrate portions were used. Plants were collected from 20 x 20 cm 2 plots (n=3), randomly positioned on the rocky boulders ( ≅1.5 m depth) and on contiguous sandy bottom ( ≅3.0 m depth). During the study period, C. scalpelliformis occurred on both substrates as a pseudo-perennial species, showing partial loss of the erect portions from winter to spring; the height and dry weight of the erect portions increased from summer to autumn on both substrates. The temporal variation of C. scalpelliformis vegetative development in Baleia Beach was similar to that described for the invasive C. racemosa and C. taxifolia from different geographical regions of the world.

R E S U M O

Caulerpa scalpelliformis cresce sobre substrato rochoso e arenoso a diferentes profundidades na Enseada de Jacuacanga, Baía da Ilha Grande, onde pode formar bancos densos. O comportamento invasor desta e de outras espécies de Caulerpa é bem documentado na literatura. Este estudo analisou a variação do desenvolvimento vegetativo de C. scalpelliformis da Praia da Baleia (23°01’63’’S e 44°14’18’’W), Enseada de Jacuacanga, de junho de 2003 a setembro de 2004, considerando plantas do substrato rochoso e do fundo de areia. Dados morfométricos e de peso seco das porções prostrada e ereta foram usados. Plantas foram coletadas em quadrados de 20 cm de lado (n=3), posicionados aleatoriamente sobre o substrato rochoso (profundidade ≅ 1,5 m) e sobre o substrato arenoso (profundidade ≅ 3,0 m). Durante o período de estudo, C. scalpelliformis ocorreu nos dois substratos como espécie pseudo-perene, mostrando perda parcial das porções eretas do talo do inverno para a primavera; altura e massa seca das porções eretas mostraram tendência de aumento do verão para o outono nos dois substratos. A variação temporal do desenvolvimento vegetativo de C. scalpelliformis na Praia da Baleia foi similar à descrita para C. racemosa e C. taxifolia , espécies invasoras em diferentes regiões do mundo.

Descriptors: Brazil, Caulerpales, Chlorophyta, Invasive species, Rocky shores, Sandy bottom, Temporal variation, Vegetative development. Descritores: Bioinvasão, Brasil, Caulerpales, Chlorophyta, Costões rochosos, Substrato arenoso, Variação temporal, Desenvolvimento vegetativo.

INTRODUCTION MITCHELL et al., 1990; NUNES, 1998). Falcão and Széchy (2005) mentioned the occurrence of Caulerpa scalpelliformis (R. Br. ex Turner) populations of C. scalpelliformis on Baleia Beach, C. Agardh (Chlorophyta, ) has been Angra dos Reis, growing in dense patches on the recorded since 1965 in the tropical regions of the rocky and sandy substrates. According to these Brazilian coast, where its distribution extends from the authors, the abundance of C. scalpelliformis increased states of Piauí to Espírito Santo (JOLY et al., 1965; on Baleia Beach from 2001 to 2003, suggesting that 146 BRAZILIAN JOURNAL OF OCEANOGRAPHY, 59(2), 2011

the species had become established in the area. Its MATERIAL AND METHODS invasive behavior was characterized by its ability to replace Sargassum vulgare C. Agardh, the dominant Baleia Beach is situated on Ponta Leste species on Ilha Grande Bay rocky shores. Figueiredo (23°01’63’’S – 44°14’18’’W), between Biscaia and and Tâmega (2007), in a survey of the diversity of the Paraíso Beaches in Jacuacanga Cove, Ilha Grande macroalgae of Ilha Grande Bay carried out in the Bay, Angra dos Reis municipality, Rio de Janeiro summer of 2003 and winter of 2004, also found C. state. Jacuacanga Cove receives domestic sewage scalpelliformis on Biscaia Beach, in Jacuacanga Cove, from Monsuaba village, a growing residential center and on Macacos Island near Ilha Grande. (personal observation). Caulerpa scalpelliformis is also recognized Access from the mainland to Baleia Beach is as an introduced and invasive species in the restricted due to the construction of private residences Mediterranean Sea (VERLAQUE, 1994; ERTAN et along the somewhat steep coastal strip; however, this al., 1998) and in Australia (DAVIS et al., 1997). beach is frequently visited by motorboats engaged in Other species of Caulerpa J. V. Lamour., such as C. tourism and fishing, looking for sheltered waters. The taxifolia (H. West in Vahl) C. Agardh and C. narrow, sandy belt of Baleia Beach is bordered by an racemosa (Forssk.) C. Agardh, are considered invasive extensive strip of rocky boulders that extends from the species in the Mediterranean Sea (BOUDOUREQUE supralittoral zone to the shallow sublittoral zone. et al., 1995; BELLAN-SANTINI et al., 1996; PIAZZI From June 2003 to September 2004, et. al., 2001; CECCHERELLI et. al., 2002; BALATA sampling was carried out along a 20 m horizontal et al., 2004; PIAZZI;BALATA, 2009), in Australia length of the sublittoral zone on the left side of (MODENA et. al., 2000) and along the Californian the sandy belt of the Baleia Beach, including the coast, USA (WILLIAMS; GROSHOLZ, 2002), rocky boulders (rocky substrate) and the because of their high rates of growth and dispersal. contiguous sandy bottom (sandy substrate). This The invasive capability of seaweed species is related location was chosen based on the previous record of to their resistance to herbivores, growth rate, Caulerpa scalpelliformis patches, both on the rocky vegetative reproduction, and successful adhesion to substrate, where it was intermingled with Sargassum different substrates, among other attributes vulgare , and on the sandy bottom (FALCÃO; (VALENTINE et al., 2007). Invasive Caulerpa SZÉCHY, 2005). species show high rates of vegetative development, On the rocky and sandy substrates, three which can be analyzed by measuring the growth of randomly positioned plots of 20 x 20 cm 2 were their erect and prostrate portions (MEINESZ et al., sampled by snorkeling at two to three month intervals. 1993; MEINESZ et al., 1995; PIAZZI et al., 2001; The rocky substrate plots were positioned at a water RUITTON et al., 2005; CEBRIAN, BALLESTEROS, depth of approximately 1.5 m, and the sandy substrate 2009). They are able to cause disturbance to the plots were approximately 3.0 m deep during high communities they invade (MEINESZ; HESSE, 1991; tides. The plots were scraped and the material VILLÈLE;VERLAQUE, 1995) because of their high collected was stored in individual plastic bags biomass and density (PIAZZI et al., 2001; THIBAUT containing a 4% formaldehyde solution. et al., 2004; KLEIN; VERLAQUE, 2008). The vegetative development of Caulerpa The marine habitats that are most susceptible scalpelliformis growing on both substrates was to the introduction of exotic benthic species are those analyzed in the different seasons using both near ports and those subject to intense and constant morphometric and dry weight data related to the erect commercial navigation. On the other hand, in areas and prostrate portions. The erect portions were that are not located near ports, the vectors for the constituted of the laminae and their stipes, and the introduction of exotic species are related to non- prostrate portions were constituted of the stolons and commercial shipping and to tourist activities such as their rhizoidal pillars (Fig. 1). fishing and aquatic recreation (HEWITT et al., 2007). For each plot, Caulerpa scalpelliformis was In Ilha Grande Bay, in addition to the presence of two separated from other organisms. Fifteen-centimeter- operating ports, a shipyard, mariculture structures, and long fragments of C. scalpelliformis stolons were many fishing villages, there is intense shipping haphazardly chosen for the morphometric analysis activity related to tourism (CREED et al., 2007). (n=5). For each C. scalpelliformis fragment, the Therefore, Ilha Grande Bay is considered to be a height of the erect portions (n=5) and the length of the favorable environment for the introduction of exotic rhizoidal pillars (n=5) were measured. species (PAULA, CREED, 2004). The dry weights of the erect and prostrate This study aimed to describe the portions of C. scalpelliformis were obtained after temporal variation of the vegetative development of drying at 80 oC to constant weight. C. scalpelliformis , growing on the rocky and sandy substrates of Baleia Beach.

VASCONCELOS ET AL.: TEMPORAL VARIATION OF Caulerpa scalpelliformis from BRAZIL 147

Fig. 1. Caulerpa scalpelliformis from Ilha Grande Bay : erect and prostrate portions of the thallus.

The temporal variation in the height and dry weight of the erect portions, the length of the rhizoidal pillars and the dry weight of the prostrate portions of Caulerpa scalpelliformis were described, in graph form, using mean and standard deviation values (n=75, 3 plots x 5 fragments x 5 measures for each fragment). Two-way analysis of variance (ANOVA) Fig. 2. Temporal variation of the erect was used for comparing the total dry weight of portions of Caulerpa scalpelliformis Caulerpa scalpelliformis (erect portions and prostrate growing on rocky substrate at Baleia Beach, portions considered together, n=3), using the type of Ilha Grande Bay, from autumn 2003 to spring 2004. 2A- Height of the erect substrate and the seasons of the years as factors, with portions (n=75, mean ± standard deviation); p<0.05 as the level of significance. This variable 2B- Dry weights of the erect portions (n=3, showed equal variance (test of equal variance, p= minimum, median and maximum values). 0.53) and normal distribution (test of normality, p= 0.33) (SIGMA STAT ® 3.5, 2006). The height of the erect portions of Caulerpa scalpelliformis from the sandy substrate reached a RESULTS maximum (15.0 cm) in autumn 2003. This variable showed a gradual increase from spring 2003 (mean= Caulerpa scalpelliformis occurred 2.29 cm) to winter 2004 (mean= 6.62 cm). A decrease throughout the year on the rocky and sandy substrates was observed from autumn (mean= 7.36 cm) to winter at Baleia Beach, Ilha Grande Bay. 2003 (mean= 2.95 cm) and from winter (mean= 6.62 The height of the erect portions of Caulerpa cm) to spring 2004 (mean= 3.20 cm) (Fig. 3A). scalpelliformis from the rocky substrate reached a The dry weights of the erect portions of maximum (12.5 cm) in winter 2003. This variable Caulerpa scalpelliformis from the sandy substrate -2 showed a gradual increase from autumn to winter in varied, on average, from 1.37 g.400cm (autumn -2 2003, and from summer to autumn in 2004. A gradual 2003) to 6.19 g.400 cm (winter 2003), when the -2 decrease was observed from winter to spring in both maximum value was reached (7.45 g.400cm ). This years (Fig. 2A). variable increased from autumn to winter in both The dry weights of the erect portions of years, and decreased from winter to spring 2003 (Fig. Caulerpa scalpelliformis from the rocky substrate 3B). The mean values of the dry weights of the erect varied, on average, from 2.07 g.400 cm -2 in autumn portions of C. scalpelliformis in winter and spring 2003 to 13.40 g.400 cm -2 in winter 2004, when the 2004 were similar, and did not coincide with the maximum value was reached (16.50 g.400 cm -2). This decrease in the heights of the erect portions for this variable increased from autumn to winter in 2003 and period. The maximum value for the dry weights of the 2004, and decreased from winter to spring in both erect portions was recorded in winter 2003, but did not years (Fig. 2B). The increase in the dry weights of the coincide with the peak in the heights of the erect erect portions from autumn (mean= 2.99 g.400 cm -2) portions in autumn 2003. On the other hand, both to winter 2004 (mean= 13.10 g.400 cm -2) did not variables behaved similarly in winter 2004, when the coincide with the variation in the heights of the erect height of the erect portions (6.6 cm) and the dry -2 portions in the same period. weight of the erect portions (6.19 g.400 cm ) reached their maximum values in that year.

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erect portions tended to increase from summer to autumn in 2004. The total dry weights of Caulerpa scalpelliformis growing on both substrates in the different seasons were compared separately for 2003 and 2004. There was a significant interaction between substrate and season; but season was the most important factor for explaining the variation of the dry weight in each year (Table 1). The length of the rhizoidal pillars of Caulerpa scalpelliformis from the rocky substrate varied, on average, from 1.05 cm (autumn 2004) to 1.70 cm (autumn 2003), but no temporal variation was detected (Fig. 4A). An increase in the dry weights of the prostrate portions of Caulerpa scalpelliformis from the rocky substrate from autumn to spring in 2003, and a gradual increase from autumn to spring in 2004 were observed (Fig. 4B). The dry weights of the prostrate portions varied, on average, from 1.00 g.400cm -2 (autumn 2003) to 7.31 g.400 cm -2 (spring 2003). The length of the rhizoidal pillars of Caulerpa scalpelliformis from the sandy substrate

varied, on average, from 1.10 cm (autumn 2004) to Fig. 3. Temporal variation of the erect 1.92 cm (winter 2004). No clear temporal variation portions of Caulerpa scalpelliformis was observed (Fig. 5A). growing on the sandy substrate at Baleia The dry weights of the prostrate portions of Beach, Ilha Grande Bay, from autumn 2003 Caulerpa scalpelliformis from the sandy substrate to spring 2004. 3A- Height of the erect varied, on average, from 0.75 g.400cm -2 (autumn portions (n=75, mean ± standard deviation); 2003) to 5.39 g.400 cm -2 (spring 2004). There was an 3B - Dry weights of the erect portions (n=3, increase from autumn to winter 2003, and a gradual minimum, median and maximum values). increase from autumn to spring 2004. From winter to On both substrates, the maximum values of spring 2003, a gradual decrease was apparent (Fig. the dry weights of the erect portions occurred in the 5B). winters of both years. In contrast, the height of the

Table 1. Results of two-factor analysis of variance (ANOVA) of total dry weight of Caulerpa scalpelliformis from Ilha Grande Bay, studied in 2003 and 2004. Factors: Substrate (rock and sand) and season (n=3). Degrees of Sum of Mean of Source of Variation Freedom Squares Squares F p value Year 2003 Substrate 1 7.566 7.566 2.332 0.153 Season 2 184.740 92.370 28.475 <0.001

Substrate x Season 2 92.495 46.248 14.257 <0.001

Residual 12 38.927 3.244 Total 17 323.727 19.043

Year 2004 Substrate 1 16.878 16.878 3.084 0.105 Season 2 230.351 115.176 21.045 <0.001

Substrate x Season 2 74.081 37.041 6.768 0.011

Residual 12 65.672 5.473 Total 17 386.982 22.764

VASCONCELOS ET AL.: TEMPORAL VARIATION OF Caulerpa scalpelliformis from BRAZIL 149

Fig. 4. Temporal variation of the prostrate portions of Fig. 5. Temporal variation of the prostrate portions of Caulerpa scalpelliformis growing on the rocky substrate Caulerpa scalpelliformis growing on the sandy substrate at Baleia Beach, IIha Grande Bay, from autumn 2003 to at Baleia Beach, Ilha Grande Bay, from autumn 2003 to spring 2004. 4A- Length of the rhizoidal pillars (n=75, spring 2004. 5A- Length of the rhizoidal pillars (n=75, mean ± standard deviation); 4B- Dry weight of the mean ± standard deviation); 5B- Dry weight of the prostrate portions (n=3, minimum, median and maximum prostrate portions (n=3, minimum, median and maximum values). values).

DISCUSSION was found in the development of the prostrate portions of C. taxifolia in the Mediterranean Sea (MEINESZ et It was possible to define a temporal al., 1995). pattern of variation for the vegetative development of Taking into account both the height and the Caulerpa scalpelliformis on Baleia Beach. This dry weight of the erect portions of the plants on sand pattern was evident in the development of the erect and rock, the decreasing trend from winter to spring portions, and can be summarized as follows: a gradual suggests the occurrence of senescence and the increase in the population from summer to autumn, subsequent loss of the erect portions, mainly the tallest and a gradual decrease in the population from winter and oldest ones. The complete or partial loss of the to spring. Similar temporal patterns have been erect portions of C. scalpelliformis may express described for other invasive Caulerpa species in other intrinsic characteristics of the population, such as the countries in different geographical regions (MODENA age and the physiological state of the thalli, and may et al., 2000; CAPIOMONT et al., 2005). However, C. also result from extrinsic abiotic and biotic factors. scalpelliformis populations did not show a clear Among the multiple abiotic factors, we may highlight temporal pattern in the development of the prostrate the impact of storms, which are more severe and portions. Similarly to our results, no temporal pattern frequent in Ilha Grande Bay during the winter period

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(PEREIRA, 1994). These storms may result in greater biomass variation of C. scalpelliformis , but the season fragmentation of C. scalpelliformis thalli was the most important factor during the two years (SANTELICES, 1977). Although the occurrence of analyzed. To define the influence of substrate type necrosis of C. scalpelliformis thalli has not been dealt and other factors on the vegetative development of the with in this study, our results suggest that necrosis and species in the study area, populations of other senescence of the erect portions are expected to occur locations in Ilha Grande Bay should be monitored, and during winter, as in other species. Meinesz and Hesse manipulative experiments should be undertaken. In (1991) and Meinesz et al. (1995) reported that necrosis agreement with a previous study in the area in C. taxifolia thalli occurred throughout the year, (FALCÃO; SZÉCHY, 2005), C. scalpelliformis is able mainly during winter. According to Klein and verlaque to grow and form dense populations in the shallow (2008), in Caulerpa racemosa populations from sublittoral zone of rocky shores of Baleia Beach, and different European regions, the number of erect also on the adjacent sandy bottom. The adaptation to portions decreases during winter, reinforcing the idea colonize different substrates is a characteristic feature of a period of senescence. The study of necrosis and of the genus. The ability to grow on different types of senescence in populations of Caulerpa species is, rocks and sand, as well as on benthic organisms, has therefore, fundamental for the understanding of their been mentioned for C. taxifolia and C. racemosa temporal variation and competitive strategy in benthic (MEINESZ et al., 1993; MEINESZ et al., 1995; communities, including the C. scalpelliformis DAVIS et al., 1997; MODENA et al., 2000; populations in Ilha Grande Bay. THIBAUT et al., 2004). The loss of erect portions during winter The capability to colonize and grow on the seems to be quickly counterbalanced from spring to sandy substrate is an important feature for the autumn, suggesting that Caulerpa scalpelliformis is dispersal of Caulerpa scalpelliformis , especially as able to regenerate and produce new erect portions regards its dispersal by fragments . In Ilha Grande Bay, continuously, during most of the year. This feature C. scalpelliformis fragments can be produced from was more pronounced in the sandy-substrate dense populations by human recreational activities population, where the height of the erect portions such as diving and fishing. Because of its calm warm increased approximately 100% from spring 2003 to waters and its beautiful landscape, Ilha Grande Bay is winter 2004. This behavior is similar to that observed the scene of the intense movement of small boats, for C. taxifolia and C. racemosa populations in the mainly during the summer (CREED et al ., 2007), Mediterranean region (MEINESZ et al., 1995; when C. scalpelliformis fragments can be transported MODENA et al., 2000; PIAZZI et al., 2001). The by anchors and fishing gear from one place to another. influence of abiotic factors such as temperature, light Recreational activities near the seaweed beds can and salinity on the growth and physiology of Caulerpa augment the fragmentation rate of their thalli and species has been investigated in laboratory-controlled promote the secondary dispersal of invasive species cultures (GACIA et al., 1996; GILLESPIE et al., (WEST et al., 2009). Therefore, it is reasonable to 1997; FRIEDLANDER et al., 2006; WEST; WEST, predict that Baleia Beach, where a dense population of 2007; BURFNEID; UDY, 2009). However, no C. scalpelliformis has been recorded on the sandy physiological data on C. scalpelliformis have yet been substrate since 2001 (FALCÃO, SZÉCHY, 2005), published. may act as a center of dispersal of this species to other At Baleia Beach, Caulerpa scalpelliformis localities in Ilha Grande Bay and also to other plants were observed throughout the 16-month study, southeastern areas with similar environmental in all the sampling periods, although there was a conditions, particularly those protected from direct partial loss of the erect portions in the winter–spring wave action, such as the northern coast of São Paulo period. This observation suggests that C. state. The vectors for the dispersal process may be scalpelliformis is a pseudo-perennial species anchors, fishing gear, and other equipments related to (MEINESZ et al., 1995). This seems to be a recreational activities in the waters of Baleia Beach. characteristic life form for the genus, because other There is another possible vector for uncontrolled species of this genus have also been described as dispersal, i.e., the culture of this beautiful and pseudo-perennials, such as C. prolifera (Forssk.) J.V. luxuriant species in aquaria, by commercial traders or Lamour. (CHAPMAN; CHAPMAN, 1976), C. by marine aquarium hobbyists (OLIVEIRA et al., racemosa (RUITTON et al., 2005) and C. taxifolia 2009). Following dispersal, C. scalpelliformis (MEINESZ et al., 1995; THIBAUT et al., 2004). populations can be successfully established on In the present study, in the light of the data different substrates, at different depths, occupying for total biomass, no preference of Caulerpa larger areas and competing with other benthic scalpelliformis for rocky or sandy substrates was organisms. Changes in the benthic community detected. The factors of substrate type and season structure are likely to occur sooner or later (FALCÃO; showed a significant interaction in affecting the SZÉCHY, 2005). The importance of thallus

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